Ruegeria strains promote growth and morphogenesis of the giant coenocytic alga Bryopsis

An evolutionarily intriguing life form among extant organisms is the giant coenocyte, exemplified by green macroalgae in the order Bryopsidales. In these algae, cell separation does not follow nuclear division, resulting in a body composed of a single multinucleated cell. How a single cell grows to over 10 cm and undergoes characteristic morphogenesis without cell division or differentiation remains poorly understood. Macroalgae are known to associate with numerous microbes, and in some cases, these interactions influence algal cell division and differentiation. Here, we show that specific bacterial strains can promote the growth and morphogenesis of the coenocytic macroalga Bryopsis. Among >100 bacterial isolates obtained from Bryopsis, four strains belonging to the genus Ruegeria were found to accelerate the growth of the main axis and induce side-branch formation when co-cultured with the alga. The same effects were observed using conditioned seawater in which Ruegeria had been pre-cultured and subsequently removed. Seasonal microbiome analysis revealed that cultured Bryopsis associates with hundreds of bacterial species, exhibiting seasonal variations in community composition. However, Ruegeria was one of the few bacterial genera consistently associated with the cultured strain, suggesting a symbiotic relationship. Notably, although Ruegeria was not detected in Bryopsis strains isolated from other regions, its effects on growth and morphogenesis were observed in co-culture experiments. These findings suggest that Bryopsis, like multicellular macroalgae, utilizes associated bacteria for growth and development without strict specificity.